Photoperiod as a Modifying and Limiting Factor in the Expression of Avian Circannual Rhythms

Abstract

In three species of birds that migrate long distances, the annual rhythms of gonadal activity, molt, and migratory restlessness (Zugunruhe ) persist for more than 1 year under certain constant conditions. The most important zeitgeber for these circannual rhythms is the annual cycle of photoperiod, which adjusts the overall period of circannual rhythms to exactly 1 year and also provides for the appropriate adjustment of seasonal activities to the temporal structure of the environment. This is illustrated by results on garden warblers (Sylvia borin) indicating that the longer photoperiods experienced by individuals wintering far south in the African wintering area phase-advance spring migration and the accompanying gonadal devel opment, relative to those of individuals wintering further north. The rate of acceleration is, however, slow enough to prevent a reproductive cycle during the Southern Hemisphere summer. Hence, endogenous circannual components and zeitgeber stimuli constitute a func tional entity that provides as a whole for adaptive temporal programming. This idea is further supported by findings in the pied flycatcher (Ficedula hypoleuca ), in which a circannual rhythmicity persists only if photoperiod in winter is at least as short as that normally encoun tered by the species in its wintering grounds slightly north of the equator. In collared fly- catchers (Ficedula albicollis), in contrast, rhythmicity continues under much longer photo periods, consistent with the fact that the wintering area of this species extends to latitudes far south of the equator. It is proposed that the adaptive function of circannual rhythms can be properly understood only if their interactions with environmental factors, particularly those that play a role as zeitgebers, are analyzed in sufficient detail. The biological significance of circannual rhythms may be more apparent in the context of the environmental constraints limiting their expression than in the often rather restricted set of conditions sustaining spon taneous annual cyclicity.

References

Aschoff, J. (1955) Jahresperiodik der Fortpflanzung bei Warmblütern . Stud. Gen. 8: 742-776.

Aschoff, J. (1960) Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 25: 11-28.

Aschoff, J. (1967) Adaptive cycles: Their significance for defining environmental hazards. Int. J. Biometeor. 11: 255-278.

Aschoff, J. (1980) Biological clocks in birds. Proc. XVII Int. Ornithol. Congr, Berling, 113-136.

Berthold, P. (1978) Circannuale Rhythmik: freilaufende selbsterregte Periodik mit lebenslanger Wirksamkeit bei Vögeln. Naturwissenschaften 65: 546.

Berthold, P. (in press) The control of migration in European warblers. Proc. XIX Int. Ornithol. Congr, Ottawa.

Berthold, P. , E. Gwinner , and H. Klein (1972a) Circannuale Periodik bei Grasmücken: I. Periodik des Körpergewichts, der Mauser und der Nachtunruhe bei Sylvia atricapilla und S. borin unter verschiedenen konstanten Bedingunger. J. Ornithol. 113: 170-190.

Berthold, P. , E. Gwinner , and H. Klein (1972b) Circannuale Periodik bei Grasmücken: II. Periodik der Gonadengröße bei Sylvia atricapilla und S. borin unter veschiedenen konstanten Bedingungen. J. Ornithol. 113: 407-417.

Bünning, E. (1956) Endogene Aktivitätsrhythmen. In Encyclopedia of Plant Physiology, Vol. 2, pp. 878-907.

10.

Chapin, J.P. (1932) The birds of the Belgian Congo, Vol. 1. Bull. Amer. Mus. Nat. Hist. 65: 1-756.

11.

Curry-Lindahl, K. (1963) Molt, body weights, gonadal development, and migration in Motacilla flava. Proc. XIII Int. Ornithol. Cong , Ithaca, pp. 960-973.

12.

Curry-Lindahl, K. (1981) Bird Migration in Africa, Vols. 1 and 2, Academic Press, London.

13.

Farner, D.S. , and B.K. Follett (1979) Reproductive periodicity in birds. In Hormones and Evolution, E. J. W. Barrington , ed., pp. 129-148, Academic Press, London.

14.

Farner, D.S. , and A.C. Wilson (1957) A quantitative examination of testicular growth in the white-crowned sparrows. Biol. Bull. 113: 254-267.

15.

Gwinner, E. (1977) Photoperiodic synchronization of circannual rhythms in the European starling (Sturnus vulgaris). Naturwissenschaften 64: 44.

16.

Gwinner, E. (1981) Circannual rhythms: Their dependence on the circadian system. In Biological Clocks in Seasonal Reproductive Cycles , B. K. Follett and D. E. Follett , eds., pp. 153-169, John Wright & Sons, Bristol, England.

17.

Gwinner, E. (1986a) Circannual Rhythms, Springer-Verlag , Berlin.

18.

Gwinner, E. (1986b) Circannual rhythms in the control of avian migrations . Adv. Stud. Behav. 16: 191-228.

19.

Gwinner, E. (1987a) Annual rhythms of gonadal size, migratory disposition and molt in garden warblers, Sylvia borin, exposed in winter to an equatorial or a southern hemisphere photoperiod. Ornithol. Scand. 18: 251-256.

20.

Gwinner, E. (1987b) Photoperiodic synchronization of circannual rhythms in gonadal activity, migratory restlessness, body weight and molt in the garden warbler (Sylvia borin). In Comparative Physiology of Environmental Adaptations, Vol. 3, P. Pévet , ed., pp. 30-44, S. Karger, Basel .

21.

Gwinner, E. (1989) Einfluß der Photoperiode auf das circannuale System des Halsbandschnäppers (Ficedula albicollis) und des Trauerschnäppers (F. hypoleuca). J. Ornithol. 130: 1-13.

22.

Gwinner, E. (in press) Photorefractoriness in equatorial migrants. Proc. XIX Int. Ornithol. Congr, Ottawa.

23.

Gwinner, E. , and J.P. Dittami (1986) Adaptive functions of circannual clocks. In Endocrine Relations as Adaptive Mechanisms to the Environment, I. Assenmacher and J. Boissin , eds., pp. 115-123, Editions du Centre National de la Recherche Scientifique, Paris.

24.

Gwinner, E. , J.P. Dittami , and J.A. Beldhuis (1988) The seasonal development of photoperiodic responsiveness in an equatorial migrant, the garden warbler Sylvia borin. J. Comp. Physiol. A 162: 389-396.

25.

Gwinner, E. , G. Gänshirt , and J. Dittami (1989) Arrhythmia in starling circannual systems : Is the clock arrested? Manuscript submitted for publication.

26.

Gwinner, E. , and I. Schwabl-Benzinger (1982) Adaptive temporal programming of molt and migratory disposition in two closely related long-distance migrants, the pied flycatcher (Ficedula hypoleuca) and the collared flycatcher (F. albicollis) . In Avian Navigation, F. Papi and H. Wallraff , eds., pp. 75-89, Springer-Verlag , Berlin.

27.

Hoffmann, K. (1981) Photoperiodism in vertebrates. In Handbook of Behavioral Neurobiology, Vol. 4, Biological Rhythms, J. Aschoff , ed., pp. 449-473, Plenum Press, New York.

28.

Marshall, A.J. , (1960a) The role of the internal rhythm of reproduction in the timing of avian breeding seasons, including migration. Proc. XII Int. Ornithol. Congr, Helsinki, pp. 475-482.

29.

Marshall, A.J. (1960b) Annual periodicity in the migration and reproduction of birds. Cold Spring Harb. Symp. Quant. Biol. 25: 499-505.

30.

Moreau, R.E. (1972) The Palaearctic-African Bird Migration System, Academic Press, London.

31.

Pengelley, E.T. , and K.C. Fisher (1963) The effect of temperature and photoperiod on the yearly hibernating behavior of captive goldenmantled ground squirrels (Citellus lateralis tescorum). Can. J. Zool. 41: 1103-1120.

32.

Pittendrigh, C.S. (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb. Symp. Quant. Biol. 25: 159-184.

33.

Pittendrigh, C.S. (1974) Circadian oscillations in cells and the circadian organization of multicellular systems. In Neurosciences: Third Study Program, F. O. Schmitt and F. G. Worden , eds., pp. 435-458, MIT Press, Cambridge, MA.

34.

Pittendrigh, C.S. (1981) Circadian systems: General perspective. In Handbook of Behavioral Neurobiology, Vol. 4, Biological Rhythms, J. Aschoff , ed., pp. 57-80, Plenum Press, New York.

35.

Rowan, W. (1926) On photoperiodism, reproductive periodicity, and the annual migrations of birds and certain fishes. Proc. Boston Soc. Nat. Hist. 38: 147-189.

36.

Saunders, D.S. (1981) Insect photoperiodism. In Handbook of Behavioral Neurobiology, Vol. 4, Biological Rhythms, J. Ascoff , ed., pp. 411-447, Plenum Press, New York.

37.

Sperlich, A. (1919) Über den Einfluß des Quellungszeitpunkts von Treibmitteln und des Lichtes auf die Samenkeimung von Alectorolophus hirsutus All., Charakterisierung der Samenruhe. S. B. Akad. Wiss. Wien, Math.-Naturwiss. Klasse I, 128: 477-500.

38.

Stetson, M.H. (1988) Processing of Environmental Information in Vertebrates , Springer, New York.

39.

Von Pernau, F.A. (1702) Unterricht was mit dem lieblichen Geschöpff, denen Vögeln, auch ausser dem Fang, nur durch Ergründung deren Eigenschaften und Zahmmachung oder anderer Abrichtung man sich vor Lust und Zeitvertreib machen könne, Nürnberg.

40.

Zink, G. (1973) Der Zug europäischer Singvögel, 1. Lieferung, Vogelzug-Verlag, Möggingen, Federal Republic of Germany.